Received: 4 June 2019 Revised: 21 October 2019 Accepted: 1 November 2019

DOI: 10.1111/conl.12684

REVIEW

Protected areas and freshwater biodiversity: a novel systematic

review distils eight lessons for effective conservation

Michael Acreman1,2 Kathy A. Hughes3 Angela H. Arthington4 David Tickner3

Manuel-Angel Dueñas1

1 Centrefor Ecology & Hydrology,

Abstract
Wallingford, UK
2 Hydro-ecology Consulting Ltd, Wallingford,
Protected areas are a global cornerstone of biodiversity conservation and restoration.
UK Yet freshwater biodiversity is continuing to decline rapidly. To date there has been
3 WWF-UK, Woking, UK no formal review of the effectiveness of protected areas for conserving or restoring
4 AustralianRivers Institute, Griffith biodiversity in rivers, lakes, and wetlands. We present the first assessment using a sys-
University, Brisbane, Australia
tematic review of the published scientific evidence of the effectiveness of freshwater
Correspondence protected areas. Systematic searches returned 2,586 separate publications, of which
Michael Acreman, Centre for Ecology & 44 provided quantitative evidence comprising 75 case studies. Of these, 38 reported
Hydrology, Crowmarsh Gifford, Wallingford,
OX108BB, UK.
positive, 25 neutral, and 12 negative outcomes for freshwater biodiversity conserva-
Email: man@ceh.ac.uk tion. Analysis revealed variable relationships between conservation effectiveness and
factors such as taxa assessed, protected area size and characteristics, International
Funding information
WWF-UK
Union for Conservation of Nature (IUCN) protected area category, and ecoregion.
Lack of effectiveness was attributed to many anthropogenic factors, including fishing
(often with a lack of law enforcement), water management (abstraction, dams, and
flow regulation), habitat degradation, and invasive non-native species. Drawing on
the review and wider literature we distil eight lessons to enhance the effectiveness
of protected areas for freshwater biodiversity conservation. We urge policymakers,
protected area managers, and those who fund them to invest in well-designed research
and monitoring programs and publication of evidence of protected area effectiveness.

KEYWORDS
conservation evidence, lakes, national parks, nature reserves, protected areas, Ramsar, rivers, systematic
review, wetlands

1 I N T RO D U C T I O N including one-third of all vertebrate species (Strayer & Dud-

geon, 2010) and more than half of all fish species (Fricke,
Freshwaters cover only approximately 0.8% of the Earth’s Eschmeyer, & van der Laan, 2019). Freshwaters also provide
surface, yet freshwater ecosystems are essential for at least important ecosystem services that support human welfare
126,000 species out of approximately 1.8 million, which and livelihoods globally (Maltby & Acreman, 2011). These
equates to almost 10% of all described species on Earth, freshwater ecosystems are embraced within the Ramsar

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original
work is properly cited.

© 2019 The Authors. Conservation Letters published by Wiley Periodicals, Inc.

Conservation Letters. 2019;e12684. wileyonlinelibrary.com/journal/conl 1 of 14

https://doi.org/10.1111/conl.12684
2 of 14 ACREMAN ET AL.

FIGURE 1 Conceptual diagram of the role of protected areas in freshwater biodiversity

Convention’s definition of wetlands (https:∖∖www.ramsar. Heritage Sites, 96 river Biosphere Reserves, and 2,314
org) that includes rivers and their floodplains, streams, lakes, listed Wetlands of International Importance (Ramsar Sites)
springs, marshes, bogs, fens, swamps, and peatlands. covering 2.42 million km2 (Ramsar, 2018b), an increase since
Despite its importance, freshwater biodiversity is contin- 1992 when there were just 575 Ramsar sites. The continuing
uing to decline rapidly at the global scale and the index of rapid decline in freshwater biodiversity globally seems at
freshwater wildlife populations has fallen by 83% since 1970, odds with this increase in protected areas, which might at
more than double the rate of species decline found in marine least have aided reduction in the rate of biodiversity decline.
and terrestrial ecosystems (WWF, 2018). More than 85% of This impasse has led to questions about the effectiveness
wetlands present in 1700 had been lost by 2000; current wet- of protected areas for freshwater species conservation and
land loss is three times faster than forest loss (Díaz, Settele, & ecosystem restoration (e.g., Pittock et al., 2015).
Brondízio, 2019). The Ramsar Convention (2018a) reported Many reasons have been suggested for the apparent lack
that wetland-dependent species, such as fish, waterbirds, and of effectiveness of protected areas for freshwater biodiversity
turtles, are in serious decline, with one-quarter threatened conservation. Not all inland water types are well-represented;
with extinction, particularly in the tropics. The Convention in fact only 10% of large rivers (Abell, Lehner, Thieme, &
on Biological Diversity (2014) concluded that pressures on Linke, 2017) and just 11% of seasonal wetlands are protected
biodiversity will increase at least until 2020, and the status of globally (Reis et al., 2017). Published explanations for weak
biodiversity is likely to continue to decline beyond that date. effectiveness include: absence of whole catchment approach
The designating of protected areas, such as national (Abell, Allan, & Lehner, 2007); limited connectivity within
parks and nature reserves, is undertaken globally to help freshwater ecosystems and with the wider landscape (Fin-
conserve and restore biodiversity (Finlayson, Arthing- layson et al., 2018); lack of protection for migratory species
ton, & Pittock, 2018) and supply ecosystem services to beyond designated areas (Bower, Lennox, & Cooke, 2014);
human societies (Dudley, Harrison, Kettunen, Madgewick, absence of control of threats beyond the protected area,
& Mauerhofer, 2016) as depicted in Figure 1. The Con- such as inflows of pollution (Adams, Setterfield, Douglas,
vention on Biological Diversity sets 20 Aichi Targets Kennard, & Ferdinands, 2015); insufficient law enforce-
(https://www.cbd.int/sp/targets/) to be met by 2020 including ment (Atkore, Sivakumar, & Johnsingh, 2011); and poor
Target 11, whereby at least 17% of global inland water areas management due to understaffing and underfunding (Le
are conserved through effectively and equitably managed, Saout, 2013). In global studies of terrestrial protected areas,
ecologically representative, and well-connected systems only 20-50% of those assessed were found to be managed
of protected areas. There are presently 39 wetland World effectively (Laurance et al., 2012). Furthermore, some 168
ACREMAN ET AL. 3 of 14

TABLE 1 Search terms and inclusion/exclusion criteria applied to capture published evidence of protected area effectiveness and to address
specific questions
Documents containing quantitative evidence of the effectiveness of protected areas for freshwater biodiversity or habitat quality were used to
answer the following questions.
Primary question: How do freshwater biodiversity and habitat change with protected area designation, design, and management?
Secondary question: What aspects of protected area designation, design, and management are most significant in changing different aspects of
freshwater biodiversity and habitat?
Ecosystems included:
Freshwater, aquatic ecosystems, deltas, estuaries, catchments, wetlands, peatbogs, peatlands, groundwater-dependent ecosystem, springs, rivers,
streams, riparian zones, floodplains, marshes, swamps, lakes, ponds, reservoirs, and canals
Ecosystem excluded :
Salt marshes, marine, saline, atmospheric, and land
Species/habitat included :
Habitat, biodiversity, wildlife, populations, endangered species, threatened species, critically endangered species, vulnerable species, birds,
waterfowl, fish, invertebrates, mammals, amphibians, frogs, reptiles, plants, macrophytes, aquatic plants, crustaceans, molluscs, fungi, insects,
dragonflies, damselflies, algae, diatoms, phytoplankton, and zooplankton
Protected areas included :
Protected areas, Ramsar sites, national parks, nature parks, nature reserves, biosphere reserves, wilderness areas, protected landscapes, world
heritage sites, Natura 2000 sites, wild scenic rivers, conservation areas, natural monuments, and management areas
Effectiveness measures included :
Comparisons, evaluations, effectiveness, consequences, conservation, maintenance, protection, enhancement, sustain, trend, benefits, restoration,
subsequent, assessment, appraisals, roles, influence, impacts, changes and performance
Inference measures included :
Previous, controls, baselines, buffers, unprotected areas, adjacent areas, before and after, inside and outside, and with and without
Precise format of search terms in Web of Science syntax is provided in Box 1, Supporting Information

Ramsar Sites within 66 countries have been formally reported undertook a systematic evidence review to answer focused
as subject to negative human-induced change or likely change questions (Table 1), by applying the Preferred Reporting
in their ecological character, an increase from 2015 when Items of Systematic reviews and Meta-Analyses (PRISMA)
there were 144 (Ramsar Convention, 2018c). (Moher et al., 2009) and guidance produced by the UK
Although numerous factors may contribute to lack of government’s Department for Environment, Food, and Rural
effectiveness of protected areas for freshwater biodiversity, Affairs (Collins, Coughlin, Miller, & Kirk, 2015). Our
there has been no systematic global review of science-based review included search and selection protocols based on
evidence on this issue (Hermoso, Abell, Linke, & Boon, the PICO (Population, Intervention, Comparator, and Out-
2016). This paper is the first to use a systematic review pro- come) framework (see Supporting Information). The search
cess to address this deficiency. It explores constraints on the strategy, search terms, and inclusion/exclusion criteria were
effectiveness of existing freshwater protected areas, and those internationally peer-reviewed and amended before searches.
incidentally protected by association with terrestrial reserves. We searched the Web of Science database (including
From this review, we define eight lessons and recommenda- SciELO) and Google Scholar, made requests to experts and
tions to enhance the conservation of freshwater biodiversity. institutions, and scanned reference lists of review papers and
books. The search terms are summarized in Table 1. These
searches returned a range of information including published
2 METHODS papers from journals and unpublished reports from conser-
vation organizations. Some documents referred to more than
Reviews are commonplace in scientific studies to estab- one species, metric, or protected area; these were recorded
lish the state of knowledge and to define future research as separate case studies. Only those containing quantitative
needs. However, reviews are often incomplete in coverage evidence of the effectiveness of protected areas for freshwater
of the literature, subjective, and biased, and the methods biodiversity or habitat quality were retained. We rejected doc-
employed opaque. To counter this, systematic evidence uments recording results of species surveys within protected
reviews were designed specifically to be comprehensive, areas but lacking comparative data outside of the area or
objective, transparent, and repeatable. They have been widely before designation. Documents that discussed concepts and
used and accepted as best practice in medical science to inferred principles but contained no new data were discarded,
develop health policies from multiple studies and are now as were documents that calculated protected area coverage
applied to environmental issues, including assessment of as percentages of geographical ranges of species but lacked
terrestrial protected areas (Geldmann et al., 2013). We information on the effectiveness of those protected areas.
4 of 14 ACREMAN ET AL.

Key information, including purpose of designation, species

protected, and broad waterbody type, was recorded for each
case study. We used the available data in each document to
define the direction of change in biodiversity or habitat and
classified each case study as positive, neutral, or negative for
freshwater biodiversity. Positive change was recorded where
freshwater biodiversity metrics in protected areas exceeded
those in comparable control areas (either the same area
before designation or in similar undesignated areas selected
by study authors). Negative change was recorded where
freshwater biodiversity metrics in comparable control areas FIGURE 2 Differences in effectiveness of protected areas (PAs)
exceed those in protected areas. Neutral change was recorded designated for terrestrial conservation, freshwater conservation, and
where metrics were similar in control and protected areas, mixed objectives for conservation of freshwater biodiversity
or before and after their designation. Additional information
about each case study, such as the International Union for for birds. The most common metrics employed were species
Conservation of Nature (IUCN) Protected Area category, abundance and richness, followed by diversity.
and the freshwater ecoregion was collated using available Detailed analysis of the effectiveness categories did not
websites and web-tools, such as Freshwater Ecoregions of highlight strong relationships with other information, such as
the World (Abell et al., 2008). the purpose of designation (e.g., for terrestrial or freshwater
conservation—Figure 2), taxa, IUCN protected area category,
or freshwater ecoregion. Success or failure depended largely
on the influence of internal (e.g., poaching) and external
3 RESULTS (e.g., catchment deforestation) pressures. Some regional
variations were evident. For example, 73% of the case studies
After removing duplications, 2,586 potentially relevant in tropical and subtropical coastal rivers showed positive
documents were retrieved. Application of selection criteria outcomes for protected areas, which exceeds the 51% overall
described above identified 44 relevant documents containing figure. Negative changes in protected area fish diversity were
75 case studies. Of the 75 case studies, 38 reported positive recorded only in studies of rivers (i.e., none for lakes, ponds,
outcomes, 25 were neutral, and 12 were negative, so 51% wetlands, or floodplains), with only 40% of case studies
showed protected areas to be effective in protecting fresh- being positive for fish diversity (Table 3). These numbers
water biodiversity. Few studies recorded reasons for positive are small and not tested for statistical significance. The main
outcomes. Many papers did not specify the management causes of negative changes were invasive non-native species,
measures employed following designation; of those that did, and disturbances from pollution and catchment degradation.
the most common were fishing restrictions and water man-
agement. Furthermore, there was no single causal factor for
3.1 Reasons given for positive and negative
lack of effectiveness (negative or neutral direction of change);
biodiversity outcomes
factors presented included fishing (often with lack of law
enforcement), water flow management (by abstraction and Several studies, including fish in Thai wetlands (reference
dams), invasive non-native species (e.g., from fish farms), 15 in Table 2) and birds on Finnish islands (26), reported
and habitat degradation (e.g., from mining or agriculture). that biodiversity increased with greater protected area size.
No case studies undertook full before–after control-impact Studies of fish in Canadian lakes (41) and plants in Aus-
(BACI) monitoring. Most (70%) compared protected with tralian wetlands (43) recommended that freshwater protected
unprotected areas, with only 20% comparing the same area area design should include the entire ecosystem (lake or
before and after designation. The case studies included sev- catchment). Other studies, for example, rivers of the southern
eral taxonomic groups, but there was a bias toward vertebrates Western Ghats, India (9) and Lake Tanganyika, Tanzania (1),
(birds 41% and fish 19%) with few studies of invertebrates concluded that although terrestrial-based protected areas did
(8%) and plants (8%). The case studies were well-distributed not adequately cover the habitat diversity of associated river
across the globe and across ecoregion categories. The highest systems, they had higher endemic freshwater species richness
numbers were from Asia, within tropical and subtropical than similar unprotected areas.
floodplain rivers and wetland complexes, IUCN category II Conserving aquatic habitat, including the hydrological
protected areas, and for fish (Table 2). The second highest regime (surface and groundwater), water quality, and riparian
numbers were from the Neotropics, within temperate flood- vegetation, was found to be vital for supporting freshwater
plain rivers and wetlands, category IV protected areas, and biodiversity worldwide, including lizards in Brazilian rivers
ACREMAN ET AL. 5 of 14

TABLE 2 Case study characteristics showing number of case studies of positive (+), neutral (0), and negative (–) biodiversity outcomes for
each region (column 1) along with details of each study (columns 2-7)
Abell et al., 2008 Freshwater
Region Change ecoregion Protected area name No. Authors Metric
Africa Positive Large lakes Gombe & Mahale 1 Britton et al. (2017) Fish diversity
4+ Large lakes Masai Mara 2 Kanga, Ogutu, Olff, Mammal abundance
30 and Santema
1– (2011)
Tropical and subtropical Various 3 Thiollay (2006) Bird abundance
floodplain rivers and wetland
complexes
Temperate coastal rivers Various 4 Kleijn, Cherkaoui, Bird abundance
Goedhart, van der
Hout, and
Lammertsma
(2014)
Neutral Large lakes Masai Mara 3 Kanga et al. (2011) Mammal abundance
Various Various 5 Kleijn et al. (2011) Bird abundance
Temperate upland rivers Maputaland–Pondoland– 6 Pryke et al., 2015 Invertebrate
Albany abundance
Negative Tropical and subtropical Chongwe & Mana Pools 7 Mutusva, Kativu, Plant density
floodplain rivers and wetland Mapaure, and
complexes Gandiwa (2016)
Asia Positive Tropical and subtropical Neyyar, Peppara, 8 Abraham and Kelkar Fish richness
16 + coastal rivers Shendurney, (2012)
50 Kulathapuzha & Palode
6–
South Western Ghats 9 Dinakaran and Invertebrate richness
Anbalagan (2007)
Invertebrate
diversity
Temperate floodplain rivers Various 10 Cui et al. (2014) Bird abundance
and wetlands
Various 11 Zhang, Jia, Prins, Bird abundance
Cao, and de Boer
(2015)
Montane freshwaters Zoige 12 Zhang et al. (2016) Net primary
production
Tropical and subtropical Katraniaghat 13 Sarkar et al. (2013) Fish diversity
floodplain rivers and wetland
complexes
Central Catchment 14 Kwik and Yeo % Native fish
(2015)
Various 15 Koning (2018) Fish biomass
Fish diversity
Fish richness
Tropical and subtropical upland Corbett & Rajaji 16 Gupta et al., 2015 Fish richness
rivers
Fish abundance
Fish body length
(Continues)
6 of 14 ACREMAN ET AL.

TABLE 2 (Continued)
Abell et al., 2008 Freshwater
Region Change ecoregion Protected area name No. Authors Metric
Temperate upland rivers Momoge 17 Jiang et al., 2016 Bird abundance
Vegetation coverage
Neutral Tropical and subtropical upland Corbett 18 Atkore et al. (2011) Fish richness
rivers
Fish abundance
Montane freshwaters Zoige 12 Zhang et al. (2016) Net primary
production
Temperate floodplain rivers various 10 Cui et al. (2014) Bird abundance
and wetlands
Tropical and subtropical Bueng Boraphet 19 Srinoparatwatana Fish diversity
floodplain rivers and wetland and Hyndes
complexes (2011)
Fish richness
Negative Temperate floodplain rivers Shengjin Lake 20 Li et al. (2015) Bird abundance
and wetlands
various 10 Cui et al. (2014) Bird abundance
Temperate upland rivers Momoge 17 Jiang et al. (2016) Bird abundance
Tropical and subtropical Central Catchment 14 Kwik and Yeo, 2015 Fish abundance
floodplain rivers and wetland
complexes
Bukit Timah 21 Ng, Yeo, Sivasothi, Invertebrate
and Ng (2015) abundance
Various 22 Sung et al. (2013) Reptile abundance
Europe Positive Temperate coastal rivers Doñana 23 Bustamante, Hydroperiod
3+ Aragones, and
20 Afan (2016)
2– Temperate floodplain rivers Grande Brière Mottière 24 Cucherousset et al. Fish production
and wetlands (2007)
Polar freshwaters Various 25 Virkkala, Poyry, Bird richness
Heikkinen,
Lehikoinen, and 7
Valkama (2014)
Neutral Polar freshwaters Various 26 Yrjola et al. (2017) Bird abundance
Temperate coastal rivers Various 27 Mancini et al. (2005) Invertebrate
biological quality
Negative Temperate floodplain rivers Various 28 Douglas et al. (2015) Burnt vegetation
and wetlands area
Temperate coastal rivers Aiguas Tortas & Lago de 29 García-Marín, Sanz, Fish frequency
San Mauricio and Pla (1998)
Neotropics Positive Tropical and subtropical upland Gama–Cabeça de Veado 30 Ledo and Colli Reptile abundance
10 + rivers (2016)
70
3–
Reptile richness
Tropical and subtropical Sete Cidades, Serra da 31 Madella-Auricchio, Reptile diversity
coastal rivers Capivara, Uruçuí-Una & Auricchio, and
Serra das Confusões Soares (2017)
Yurubí 32 Rodríguez-Olarte Fish richness
et al. (2006)
(Continues)
ACREMAN ET AL. 7 of 14

TABLE 2 (Continued)
Region Change Abell et al., 2008 Freshwater Protected area name No. Authors Metric
ecoregion
La Selva 33 Snyder, Pringle, and Invertebrate
Tiffer-Sotomayor abundance
(2013)
Calakmul 34 Vega-Cendejas, Fish abundance
Santillana, and
Norris (2013)
Tropical and subtropical Los Amigos 35 Pitman et al. (2011) Bird abundance
floodplain rivers and wetland
complexes
Mammal abundance
Reptile abundance
Large river deltas Amapá 36 Norris et al. (2018) Reptile egg
predation by
humans
Neutral Tropical and subtropical Pantanal 37 Penha et al. (2014) Fish biomass
floodplain rivers and wetland
complexes
Fish diversity
Fish richness
Fish abundance
Tropical and subtropical Calakmul 34 Vega-Cendejas et al. Fish diversity
coastal rivers (2013)
Fish richness
Large river deltas Amapá 38 Arraes and Reptile egg
Tavares-Dias predation by
(2014) humans
Negative Temperate coastal rivers Carlos Anwandter 39 González and Fariña Bird abundance
(2013)
Large river deltas Amapá 36 Norris et al. (2018) Reptile egg
predation by
humans
Tropical and subtropical Yurubí 32 Rodríguez-Olarte Fish abundance
coastal rivers et al. (2006)
North Positive Temperate floodplain rivers Voyageurs lakes 40 Christensen and Chlorophyll a
America and wetlands Maki (2015)
4+ Large lakes Various 41 Chu et al. (2018) Fish length
50 Temperate upland rivers Theodore Roosevelt 42 Hossack, Corn, and Amphibian richness
0– Pilliod (2005) Reptile richness
Neutral Temperate floodplain rivers Voyageurs National Park 40 Christensen and Depth transparency
and wetlands lakes Maki (2015) Total phosphorus
Chlorophyll a
Large lakes Various 41 Chu et al. (2018) Fish abundance
Fish diversity
Oceania Positive Tropical and subtropical Kakadu Park 43 Adams et al. (2015) Vegetation coverage
1+ coastal rivers
20
0–
Neutral Temperate floodplain rivers Various 44 Chessman (2013) Fish abundance
and wetlands
Fish richness
8 of 14 ACREMAN ET AL.

TABLE 3 Relationship between broad water body type and of shrimps in Costa Rica (33) and of eels in France (24).
direction of change (for studies involving fish metrics only) In Brazil, community-based management approaches have
Direction of change succeeded in reducing poaching of turtle eggs, where formal
Negative Neutral Positive Total law enforcement had previously failed (36).
River 3 3 4 10 Many factors influenced the natural distributions of
Lake 0 2 2 4 species, their abundance, and freshwater biodiversity, includ-
Wetland 0 2 1 3 ing ecoregion, variations in the landscape, river channel
Floodplain 0 4 0 4
morphology, water quality, flow regime, and climate. In
some cases, these factors had more influence on biodiversity
Pond 0 2 1 3
than protected area status and management, including Aus-
Total 3 13 8 24
tralia’s Murray–Darling Basin (43), streams in Italy (27) and
Singapore (21), karstic pools in Mexico (34), and waterbird
(30), fish in karstic pools in Mexico (34), birds in Chinese habitats in Morocco (4).
rivers (17), and wetlands in Spain (23). Disconnection of
the River Yangtze from its floodplain was a partial cause 4 LES S O NS TO ENH ANCE
of reduced numbers of cranes in a reserve in China (20). P ROTECTED AREA
Lowering of the groundwater table contributed to degradation EF F ECTIVENES S
of vegetation in National Parks in Zambia (7). These studies
demonstrate the importance of lateral (e.g., river-riparian and Although the information base is limited, our novel applica-
floodplain zones) and vertical (e.g., surface–groundwater) tion of the systematic review process has produced evidence
connectivity. The lack of systematic protection of different that protected areas can be effective for conservation and
habitats and pathways for migratory fish (e.g., for spawning, restoration of freshwater biodiversity. However, almost half
larvae, juveniles, and adults) is highlighted in the general lit- of the 75 case studies were not effective. We distilled the
erature (Mcintyre et al., 2016). However, no studies directly evidence into eight lessons for improving protected area
observed lack of longitudinal connectivity (upstream– assessment, design, and management to enhance freshwater
downstream) as the main cause of negative outcomes for conservation effectiveness. Our lessons build on many previ-
freshwater biodiversity in protected areas, although several ous works (e.g., Adams et al., 2015; Fiedler & Karieva, 1997;
authors inferred the possibility in discussion. Hermoso et al., 2016, 2018; Strayer & Dudgeon 2010) and
The need to reduce pressures in and around protected strengthen their essential messages by providing empirical
areas from grazing, inappropriate land and water manage- evidence from the systematic literature search.
ment, pollution, tourism, or general human disturbance was
emphasized in studies of wetlands in Tibet (12) and the
4.1 Lesson 1: Monitoring and research to
United States (42), aquatic insects in India (9), and birds in
understand effectiveness should be built into
China (20). Catchment disturbances (dredging, mining, and
management of protected areas
deforestation) were found to impact biodiversity in protected
rivers in Venezuela (32), Kenya (2), and Italy (27), and in This review selected 44 papers (from 2,586 retrieved)
wetlands across Africa (5), but protected areas were shown containing only 75 case studies (of the many thousands of
to be effective buffers from adverse external pressures for protected areas worldwide) based on quantitative evidence of
reptiles in Brazilian rivers (30) and fish in Indian rivers (16). changes in freshwater biodiversity that stem from protected
Three river studies reported reductions in endemic and area designation. The limited evidence base means there
other native species within protected areas caused by invasive is possibly weak understanding of the conditions under
non-native species. In Mexico (34), flooding during the which protected area succeed or fail to deliver freshwater
rainy season allowed tilapia to escape from fish farms. In conservation (Geldmann et al., 2013). Factors influencing
Spain (29), non-native fish species had a greater impact on the scarcity of evidence include constraints on study design,
protected areas than in fished areas, suggesting the need for in particular the difficulty of finding comparable unprotected
different management strategies in the two. An Australian areas (i.e., control or reference aquatic systems), and the
case study (43) reported that control of invasive plants was a challenges of conducting before–after studies, especially
major objective. BACI designs, which arguably require longer timeframes to
Lack of law enforcement in protected areas contributed detect biodiversity outcomes in freshwater systems with high
to the decline of turtles in Hong Kong streams (22), birds natural temporal variability (Adams et al., 2015). Monitoring
in African wetlands (5), and fish in Indian rivers (16). In outcomes in protected areas can be expensive (Hockings,
contrast, protection had reduced hunting of reptiles, birds, Stolton, Leverington, Dudley, & Courrau, 2006) and demands
and mammals in the Amazon, Peru (35) and over-fishing rigor to capture biodiversity responses.
ACREMAN ET AL. 9 of 14

Although invertebrates make up the bulk of freshwater evidence of positive outcomes for freshwater biodiversity,
animal diversity, in both taxonomic and functional contribu- such as higher fish diversity in areas of Lake Tanganyika
tions, they are poorly represented in assessments of protected designated for conservation of terrestrial species (Britton
area effectiveness, with a strong bias toward monitoring et al., 2017) and greater numbers of threatened fish species
vertebrates. We recommend monitoring a wider range of in rivers within Indian tiger reserves than in areas outside of
faunal groups as well as plants and algae. Further work is terrestrial reserves (Gupta, Sivakumar, Mathur, & Chadwick,
also necessary to define new metrics for measuring fresh- 2015). In another study, three of four pollution-intolerant fish
water protected area effectiveness that capture spatial and species were more abundant in lakes with partially protected
temporal variations in ecological processes and responses shorelines (Chu, Ellis, & de Kerckhove, 2018); here, fish
to common stressors, as well as typical metrics of change in populations would benefit from protected areas that include
biodiversity or the abundance of particular taxa (Hermoso the entire lake rather than protecting just part of the shoreline.
et al., 2016, 2018). Greater recognition of variability and Likewise, extending the scope of terrestrial protected areas
time lags in population and community responses could help to incorporate freshwater ecosystems would benefit narrow-
us understand why some protected area assessments reveal range endemic fishes in the Western Ghats, India (Abraham
positive biodiversity outcomes and others do not (Adams & Kelkar, 2012). These studies indicate the potential to
et al., 2015; Geist, 2015). It is also essential to monitor derive biodiversity benefits for freshwater systems within or
the many environmental factors that vary naturally, such as bordered by terrestrial protected areas by extending design
climate, geology, soils, vegetation, and water flows, as these features to include more aquatic habitat diversity, and by
influence biodiversity in both protected and unprotected reducing threats (e.g., sand mining, dynamite fishing, pollu-
areas. We reiterate calls for a step change involving increased tion, and introduced invasive fishes) that affect aquatic biota.
monitoring and research in protected areas. We suggest that such opportunities merit more attention in
regions where declaration of dedicated freshwater protected
areas may be unlikely or beyond resource capacity, yet benefi-
4.2 Lesson 2: Protected areas need to be of cial adjustments and more sensitive management of terrestrial
sufficient size and configuration to connect protected areas may help to conserve freshwater biodiversity.
diverse elements of the waterscape and
maintain their biodiversity
This study records evidence that greater protected area size
4.4 Lesson 4: Incorporating conservation of
and habitat heterogeneity enhance biodiversity outcomes for
aquatic habitats, including hydrological regime,
invertebrates in ponds and fish in wetlands (Pryke, Samways,
water quality, and riparian vegetation, into
& De Saedeleer, 2015; Koning, 2018). In riverine systems,
protected area strategies is vital to maintaining
many fish species use different habitats and parts of the basin
freshwater biodiversity
at different life stages, often migrating significant distances to Freshwater habitats vary widely in character, spatial patterns,
maximize population potential (Mcintyre et al., 2016). Protec- and temporal dynamics and many physical, chemical, and
tion of each habitat and connecting pathways is essential for biological factors govern their potential to support freshwater
their survival and recruitment (Hermoso, Filipe, Segurado, & biodiversity. The hydrological regime is a defining feature,
Beja, 2018). Lack of multi-direction connectivity, including governing channel structure and connectivity, substrate
longitudinal, lateral (river to riparian and floodplain habitats), characteristics, and aquatic habitat features important to
vertical (surface-groundwater), and temporal connectivity, invertebrates and fish as shelter, sources of food, and spawn-
may compromise biodiversity protection (Linke, Turak, ing sites. The need for integrated management of water
& Nel, 2011). We recommend application of systematic resources to sustain flowing, standing, and groundwater-
conservation planning principles and modelling techniques dependent ecosystems is recognized in frameworks such as
(e.g., Grantham et al., 2016; Howard et al., 2018) during the environmental flow management (Arthington et al., 2018),
placement, design, and gazettal of freshwater protected areas. Integrated Lake Basin Management (ILBM), and Integrated
Water Resources Management (IWRM). Aquatic habitats
typically interface with a riparian or littoral zone where
4.3 Lesson 3: Areas designated to protect
stands of semi-aquatic and terrestrial vegetation regulate
terrestrial ecosystems can contribute to
shading and water temperature, channel stability, and supplies
freshwater biodiversity protection if they are
of nutrients and organic matter to aquatic food webs (Naiman
located, designed, and managed appropriately
et al., 2005). These habitat features contributed to positive
Large areas set aside to protect terrestrial biodiversity, such fish diversity outcomes in protected areas of Indian rivers
as national parks, often do not protect freshwater biodiversity (Sarkar et al., 2013) and lizard diversity in Brazilian riparian
(Grantham et al., 2016). However, our review found new forests (Ledo & Colli, 2016). Maintaining the heterogeneity
10 of 14 ACREMAN ET AL.

of aquatic habitat structure and the natural factors that influ- 4.6 Lesson 6: Well-managed protected areas
ence spatial scales and temporal dynamics of habitat within can provide a refuge for native species against
protected areas is essential to protect freshwater biodiversity. invasive non-native species
Introductions of aquatic fauna occur through, for example,
4.5 Lesson 5: Protected areas should be free bait-bucket releases by anglers, deliberate introduction of
of external and internal pressures from favored game fish, and escapes from the ornamental fish
inappropriate, illegal, or unregulated land and trade, fish farms, and ornamental ponds. de Poorter, Pagad,
water management and Irfan Ullah (2007) found that 277 Ramsar sites (17% of all
Ramsar sites) were threatened by invasive non-native species.
Most freshwater ecosystems are influenced, usually adversely,
Invasive species can alter habitat structure, the demography of
by human disturbance of the natural characteristics of the
native plants, fish and invertebrates, community composition,
catchment in which they are situated, including changes to
and the genetic characteristics of species through hybridiza-
water flow regimes and basin-scale connectivity, production
tion. Although the problem may worsen as species ranges
of excess sediment, nutrients and toxic pollutants (Linke
alter in response to climatic shifts, Gallardo et al. (2017) pre-
et al., 2011), and landscape modifications, such as deforesta-
dicted that protected areas will provide some refuge for native
tion and logging, livestock grazing, cropping, salinization,
species, particularly in remote and pristine regions with very
and urbanization (Dudgeon et al., 2006, Rodríguez-Olarte,
low human accessibility and density. Protected areas with
Amaro, Coronel, & Taphorn, 2006). The overriding detri-
high human accessibility and density are more likely to expe-
mental influence of catchment land use meant that creation
rience new invasive species and expanding invasion fronts.
of protected areas per se did not increase macroinverte-
We recommend preventing, removing, or controlling invasive
brate diversity in Italian rivers (Mancini et al., 2005). In
non-native species (particularly those that cause detriment or
African wetlands, bird populations did not differ significantly
loss of native species), maintaining aquatic conditions that
between Ramsar sites and non-designated sites, due to
favor native species (e.g., “natural” flow regimes and habitat
habitat degradation associated with increasing arable areas,
connectivity) and manipulating conditions that suppress
livestock numbers, and deforestation in surrounding lands
invasive non-native species (e.g., water level and temperature
(Kleijn et al., 2011). For these reasons, management needs to
fluctuations during fish spawning). We also recommend more
extend beyond the limits of the freshwater ecosystem and to
effort to recognize, disrupt, and monitor pathways by which
include at least some of the upstream catchment and drainage
non-native flora and fauna can enter protected areas, and
network, the riparian zone, and downstream reaches, and
strategies to limit new introductions and control populations
maintain habitat patchiness, connectivity pathways, and
within, connected to, or near to protected freshwater systems
associated ecological processes (Dudgeon et al., 2006).
(Genovesi & Monaco, 2013), such as prohibition of live fish
Where protection of large portions of a multi-use catchment
transport, barriers to movement, and selective fish traps (e.g.,
is not practical, we recommend riparian and catchment
Asian Carp Regional Coordinating Committee 2019).
zoning (Abell et al., 2017; Sheldon et al., 2012) prescribing
different management regimes consistent with conservation.
Human activities within protected areas can also generate
4.7 Lesson 7: Meeting socioeconomic
disturbances that constrain biodiversity outcomes. This rev-
protected areas objectives, such as grazing,
iew recorded negative changes in river fish metrics within pro-
tourism, and recreation, may result in a
tected areas due to local disturbances from dredging, mining,
tradeoff against biodiversity
and deforestation (Rodríguez-Olarte et al., 2006). Chemical
contamination from a pulp mill that triggered the disappear- The effectiveness of many freshwater protected areas is
ance of Brazilian waterweed, the food plant of black-necked compromised by explicitly aiming to meet diverse human
swan (Cygnus melancoryphus), caused high mortalities due expectations other than biodiversity conservation and sup-
to starvation as well as massive migration out of the protected porting activities such as recreational hunting, fishing,
area (González & Fariña, 2013). Illegal fishing and harvesting boating, and livestock grazing. Freshwater ecosystems are
of turtle eggs and adults within protected areas has reduced a major focus of visitor activities and most protected areas
biodiversity in Amazon rivers (Norris, Michalski, & Gibbs, require management of the trade-offs between freedoms of
2018). We recommend prohibitions or limitations on external visitor use, benefits in terms of revenue for park management,
and internal threatening processes, coupled with monitor- the health and cultural benefits for visitors, and biodiversity
ing and research to quantify how much disturbance from conservation. Burning carbon-rich upland heath and blanket
particular forms of catchment land-use change and internal bogs (moorland) in the UK to promote gamebird shooting, and
threats can be tolerated without compromising biodiversity to a lesser extent livestock grazing, is likely to be detrimental
and ecosystem resilience in freshwater protected areas. for soil carbon storage, water quality, and habitat condition
ACREMAN ET AL. 11 of 14

in conservation areas, as well as having implications for (Hermoso et al., 2016), limiting our ability to define principles
climate change and wider biodiversity (Douglas et al., 2015). and practices to enhance freshwater conservation. Our novel
Wetland losses and habitat degradation associated with aqua- application of the systematic review process has produced
culture within important protected areas on Yangtze River results that build on many previous works (e.g., Abell et al.,
floodplains have led to decline of the hooded crane (Grus 2017; Dudgeon et al., 2006; Fiedler & Karieva, 1997; Fin-
monacha), listed as Vulnerable on the IUCN Red List (Li, layson et al., 2018; Reis et al., 2017; Strayer & Dudgeon 2010)
Zhou, Xu, Zhao, & Beauchamp, 2015). Surrounding paddy and our eight lessons reiterate and reinforce their essential
fields provide alternative feeding grounds but even within messages. They complement the findings of a similar review
this buffer zone the feeding behaviors and energetic benefits of terrestrial protected area effectiveness, in particular the
for cranes and other migratory waterbirds are compromised influence of human activities on biodiversity and governance
by human disturbances. We recommend more effort to ensure issues (Blanco et al., 2019). The review has revealed evidence
that any socioeconomic objectives of protected areas are from quantitative case studies that not all protected areas
consistent with maintenance or restoration of ecosystem have been effective for freshwater biodiversity conservation.
resilience and conservation of freshwater biodiversity. Nevertheless, there is great potential to improve effectiveness
and to enhance its contribution to the conservation and
4.8 Lesson 8: Laws and regulations restoration of freshwater biodiversity. We urge policymakers,
associated with protected areas need to be protected area managers, and those who fund them to invest in
enforced, but regulation activities should well-designed research and monitoring programs, collection
involve engagement of local communities of relevant spatial and temporal data on a wider range of
taxonomic groups and ecological processes, and publication
Controversy exists over the best way to ensure that protected of evidence of protected area effectiveness, or the lack
areas meet their objectives in the face of pressures for resource thereof. The eight lessons and recommendations arising from
use from local communities. Many argue that strict protection this systematic review offer many opportunities to strengthen
by law enforcement is the most promising approach, whereas the conservation effectiveness of freshwater protected area
Borrini-Feyerabend et al. (2013) suggest that the institutions designs, management, and socio-ecological trade-offs, but
and rules governing protected areas should be embedded in only if we have the resolve to support and implement them
societal norms and adaptive to changing challenges. Protected rigorously, collaboratively, and much more widely.
areas producing positive socioeconomic outcomes are more
likely to report positive conservation outcomes (Oldekop
ACKNOW LEDGMENTS
et al., 2016) and the success of Ramsar sites improved
with increased participation of local stakeholders (Castro, The work was initiated, funded, and managed by WWF-UK
Chomitz, & Thomas, 2002). Big-headed turtles (Platysternon from a grant provided by HSBC. Data were gathered from
megacephalum) were more numerous in a private refuge in published papers available on the internet. All aspects of the
Hong Kong than in national parks as a result of fencing and work followed ethics policies of WWF.
frequent patrols both day and night (Sung, Karraker, & Hau,
2013). Greater numbers of threatened fish species occurred
R E F E R E NC E S M E E T I NG R E V I E W
in rivers within tiger reserves in India because illegal fishing,
SELECTION CRITERIA
diversion of water, clearing of riparian vegetation, and sand
mining were all lower than in areas that lacked legislative, Abraham, R. K., & Kelkar, N. (2012). Do terrestrial protected
religious, or socioeconomic drivers of protection (Gupta areas conserve freshwater fish diversity? Results from the West-
et al., 2015). In Brazil, community-based management ern Ghats of India. Oryx, 46(4), 544–553. https://doi.org/10.1017/
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Adams, V. M., Setterfield, S. A., Douglas, M. M., Kennard, M. J., &
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Protected areas have been cornerstones of biodiversity of diversity and conservation status of freshwater fishes in the tribu-
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